Role of caveolae in signal-transducing function of cardiac Na+/K+-ATPase

Am J Physiol Cell Physiol. 2003 Jun;284(6):C1550-60. doi: 10.1152/ajpcell.00555.2002. Epub 2003 Feb 26.

Abstract

Ouabain binding to Na(+)/K(+)-ATPase activates Src/epidermal growth factor receptor (EGFR) to initiate multiple signal pathways that regulate growth. In cardiac myocytes and the intact heart, the early ouabain-induced pathways that cause rapid activations of ERK1/2 also regulate intracellular Ca(2+) concentration ([Ca(2+)](i)) and contractility. The goal of this study was to explore the role of caveolae in these early signaling events. Subunits of Na(+)/K(+)-ATPase were detected by immunoblot analysis in caveolae isolated from cardiac myocytes, cardiac ventricles, kidney cell lines, and kidney outer medulla by established detergent-free procedures. Isolated rat cardiac caveolae contained Src, EGFR, ERK1/2, and 20-30% of cellular contents of alpha(1)- and alpha(2)-isoforms of Na(+)/K(+)-ATPase, along with nearly all of cellular caveolin-3. Immunofluorescence microscopy of adult cardiac myocytes showed the presence of caveolin-3 and alpha-isoforms in peripheral sarcolemma and T tubules and suggested their partial colocalization. Exposure of contracting isolated rat hearts to a positive inotropic dose of ouabain and analysis of isolated cardiac caveolae showed that ouabain caused 1) no change in total caveolar ERK1/2, but a two- to threefold increase in caveolar phosphorylated/activated ERK1/2; 2) no change in caveolar alpha(1)-isoform and caveolin-3; and 3) 50-60% increases in caveolar Src and alpha(2)-isoform. These findings, in conjunction with previous observations, show that components of the pathways that link Na(+)/K(+)-ATPase to ERK1/2 and [Ca(2+)](i) are organized within cardiac caveolae microdomains. They also suggest that ouabain-induced recruitments of Src and alpha(2)-isoform to caveolae are involved in the manifestation of the positive inotropic effect of ouabain.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Animals, Newborn
  • Caveolae / chemistry
  • Caveolae / metabolism*
  • Caveolin 1
  • Caveolin 3
  • Caveolins / metabolism
  • Cell Fractionation
  • Cells, Cultured
  • Enzyme Inhibitors / metabolism
  • ErbB Receptors / metabolism
  • Humans
  • In Vitro Techniques
  • Mitogen-Activated Protein Kinases / metabolism
  • Myocardial Contraction
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism*
  • Ouabain / metabolism
  • Protein Subunits / isolation & purification
  • Protein Subunits / metabolism*
  • Rats
  • Signal Transduction / physiology*
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Swine
  • src-Family Kinases / metabolism

Substances

  • CAV1 protein, human
  • Cav1 protein, rat
  • Cav3 protein, rat
  • Caveolin 1
  • Caveolin 3
  • Caveolins
  • Enzyme Inhibitors
  • Protein Subunits
  • Ouabain
  • ErbB Receptors
  • src-Family Kinases
  • Mitogen-Activated Protein Kinases
  • Sodium-Potassium-Exchanging ATPase